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BASIC AND CLINICAL RESEARCH

Effects of Electromagnetic Field on Bone Healing Around Commercially Pure Titanium Surface: Histologic and Mechanical Study in Rabbits

Buzzá, Edmur Pereira DDS, MS*; Shibli, Jamil Awad DDS, MS**; Barbeiro, Roberto Henrique DDS, PhD, MS***; Barbosa, José Ricardo de Albergaria DDS, PhD, MS

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doi: 10.1097/01.ID.0000058385.23346.4D
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Abstract

The use of dental implants to restore partially or totally edentulous patients has been documented with success rates of up to 90% over a 10-year period. 1 In spite of these high success rates, many inadequacies (not only absence of primary stability but also lack of long-term success) may occur due to low bone quality present in some patients. The development of dental implant surfaces (microstructure) such as sandblasted surfaces and hydroxyapatite coating, as well as some clinical procedures such as early immediate loading and the use of platelet-rich plasma, have been developed to accelerate the osseointegration in dental implantology, decreasing the long period between implantation and prosthetic rehabilitation.

Some studies have suggested the application of a pulsed electromagnetic field (PEMF) in the bone-healing process in orthopedic treatment and in oral implantology. 2–4 The mechanism by which PEMF stimulates osteogenesis has not yet been established, but it is believed that stimulation is able to promote vascularization, collagen production, and/or osteogenic cell proliferation and differentiation. 4–6 However, all studies evaluated porous surfaces or hydroxyapatite coating implants. The purpose of this study was to investigate the performance of the bone-healing process around commercially pure titanium implants subjected to extraction forces after insertion in rabbit tibiae on PEMF stimulation as well as the cortical and endosteal histologic characteristics.

Materials and Methods

Animals and Dental Implants

Twelve New Zealand adult female albino rabbits were used for the experiment. The rabbits were anesthetized with 5.5 mg/kg Ketalar (Laboratório Park-Davis, Brazil), 5 mg/kg Rompum (Bayer do Brazil SA, São Paulo, Brazil), and 0.1 mL/kg atropine sulphate (Ariston Quimica e Farms. LTDA, São Paulo, Brazil) according to standard procedures. After cutaneous incision, subcutaneous tissue and muscular planes were dissected to expose tibiae metaphysis. Two cylindrical preparations were drilled per tibia in order to tightly house a commercially pure titanium fixture 6 mm long and 2.6 mm in diameter (INP, National Implants System, São Paulo, Brazil), totaling 48 dental implants.

Muscular planes and cutaneous tissues were then sutured, and an antibiotic coverage with potassic and sodic benzylpenicillin (Pentabiótico Veterinário, Fort Dodge Saúde Animal LTDA, São Paulo, Brazil) was administered to the animals.

Application of PEMF

A PEMF generator (Healtec-Celular, Healtec Eletromedicina Ltd., Brazil) connected to a band coil, with pulse width of 85 μs and a pulse frequency of 20 Mc, was used. The action depth was 25 cm with 1 W of potency. Rabbits that were not treated with PEMF served as controls. PEMF stimulation was initiated 24 hours after the implantations. Both tibias of the rabbit were placed in a circular space of the band coil and stimulated during 30 minutes, for 21 and 42 days. 7 The control group was placed in a circular place but did not receive stimulation.

Specimen Retrieval and Removal Torque

After 21 and 42 days, the animals with implants were anesthetized, and one joint implant and one tibial implant were each fully unscrewed with a torque gauge manometer (Dremometer Rahsol, Gedore, Germany). To connect the torque meter, bone or cartilage that had formed on the top of the implants was carefully removed using a scalpel and a fissure bur. When an implant was unscrewed, the peak torque value fell quickly when the rupture between bone and implant occurred. Up to this moment no macroscopic movement of the implant was evident. After rupture, the continued unscrewing required low torque.

Following, the tibiae metaphysis were carefully dissected and the block biopsies were harvested, fixed in buffered formalin, and decalcified in Morse solution. Once decalcified, biopsies following routine histologic processing and paraffin embedding were done and 6-μm thick tissue blocks on the longitudinal plane were obtained. For each biopsy, sections were selected in the central portion of the bone cores. These selected sections were stained with Harris hematoxylin and 1% eosin and Masson trichromic.

The mechanical data was subjected to analysis of variance and treatment comparisons were made using the F test (P > 0.05).

Results

All animals recovered well after surgery with no postoperative complications. Only normal postoperative swelling and hematoma formations were observed. On the day the animals were killed there were no macroscopic signs of inflammation. After 42 weeks, some implants were covered by newly formed bone.

Torque Measurements

The torque required to unscrew the dental implants ranged between 8.87 ± 0.64 and 9.42 ± 1.27 Ncm for the control and PEMF group at 21 days, respectively. These means increased significantly (P < 0.0001) over time in the control (14 ± 3.69 Ncm) and PEMF (14.38 ± 2.38 Ncm) groups, in that more torque was needed to unscrew the dental implants of both groups. However, statistically significant differences were not observed between groups (P > 0.05) after the experimental periods (Table 1).

Table 1
Table 1:
Analysis of Variance for Comparison of Torque Measurements Over Time Within and Between Groups

Morphology

After 21 days, histological evaluation revealed the presence of new bone with compact and cancellous areas for both groups (Figs. 1 and 2). The medullary spaces were ample and almost always filled with a well-vascularized connective tissue with no signs of inflammation in the control group. The PEMF group presented medulla-filled bone marrow cells and small bony islets together with vascularized connective tissue.

Fig. 1
Fig. 1:
Longitudinal section through the middle portion of the control group specimen at 21 days. The area limited by arrow shows incremental basophilic lines mixed with interposed reversion lines the reversal line (Original magnification 100x, HE).Fig. 2. Decalcified section of test group depicted compact areas and new bone formation in the threads area (arrow) at 21 days. (Original magnification 100x, HE). Fig. 3. Section obtained form control group (42 days) show reversion lines as well as new bone formation (arrows). (Original magnification 160x, Masson trichromic). Fig. 4. Aspect from test group at 42 days. The compact areas, incremental basophilic lines (arrows) and medullary spaces filled with connective tissue. (Original magnification 100x, HE). Fig. 5. Section decalcified depicted test group (42 days) new bone formation at threads area and reversion lines (arrows). Note the ample vascularized aspect in this specimen. (Original magnification 160x, Masson trichromic). Fig. 6. Specimen from control group at 21 days show small bony islet (arrows). (Original magnification 100x, HE).

At 42 days, the cancellous bone exhibited as the compact areas, incremental basophilic lines mixed with interposed reversion lines. This characteristic was not accentuated in any group (Figs. 3 and 4). The bone-formation process was well identified by the presence of osteoblasts and the Haversian system was well-formed after 42 days (Fig. 5). Morphological differences between test and control groups were not observed. The medullary spaces were most vascularized at 21 days for both groups, at which time some specimens from the control group showed small bony islets (Fig. 6).

Discussion

Pulsing electromagnetic fields of differing waveforms and frequencies have been applied successfully in the treatment of congenital and acquired pseudoarthroses and nonunion fractures. 4,8,9 PEMFs alter the deposition, quantity, and composition of extracellular matrix, as well as inhibit bone cell responsiveness to parathyroid hormone and osteoclast activation factor. 10,11 Ryaby et al 2 have proposed that magnetic fields stimulate secretion of insulinlike growth factor II after a short duration of electromagnetic stimulus, and advise that the prolonged effects of electromagnetic stimuli should be mediated by a growth factor dependent mechanism.

This study failed to show an increase in bone formation around commercially pure titanium surface implanted in PEMF rabbits when compared to a control group. Shimizu et al 12 observed the bone ingrowths into titanium and hydroxyapatite-coated surfaces, and Matsumoto et al 3 showed bone growth in titanium-blasted surfaces. Our data do not show any morphological differences between the experimental and control groups. The roughness of the implant surface used by Shimizu et al 12 and Matsumoto et al 3 may explain the different results observed in our study. The blasted surface and hydroxyapatite-coated surfaces may provide better stability for the coagulum that forms in the recipient site following the implant insertion; and that in turn may promote healing and facilitate the maturation of a provisional connective tissue and finally the deposition of the bone. 8,13 The amount of bone formed in different implant surfaces is well documented in literature. 14,15 This statement is in accordance with Matsumoto et al 3 In that paper, the authors suggested that PEMF might be used to promote bone formation on porous as well as rough-surfaces. Shimizu et al 12 suggest that hydroxyapatite-coated surfaces presented a better degree of vascular invasion than commercially pure titanium surfaces.

Factors such as the duration of stimulation and intensity of electromagnetic powers are still controversial. 2,11 These factors may also explain the differences in the results of our study and that conducted by Matsumoto et al. 3 In addition, the bone formation adjacent to dental implant surfaces appeared to be similar for both groups; both in the cortical and medullar regions.

Conclusion

Within the limits of this study, it can be concluded that there was no quantitative, statistically significant difference in torque between the PEMF and control groups. The histologic features did not differ between groups, suggesting that CP dental implant surfaces do not promote better bone formation when submitted to PEMFs.

Disclosure

The authors claim to have no financial interest in any company or any products mentioned in this study.

Acknowledgments

This research project was supported by FAPESP grant No. 97/12945–5. The authors greatly appreciate the assistance of Dr. José T. T. Siqueira (INP, São Paulo, Brazil) for supplying the dental implants.

References

1. Apse P, Zarb GA, Schmitt A, et al. The longitudinal effectiveness of osseointegrated dental implants. The Toronto study: Peri-implant mucosal response. Int J Periodont Rest Dent. 1991; 11: 95–111.
2. Ryaby JT. Clinical effects of electromagnetic and electric fields on fracture healing. Clin Orthop. 1998; 355s: 205–215.
3. Matsumoto H, Ochi M, Abiko Y, et al. Pulsed electromagnetic fields promote bone formation around dental implants inserted into femur of rabbits. Clin Oral Implants Res. 2000; 11: 354–360.
4. Basset CAL, Valdes MG, Hernandez E. Modification of fracture repair with selected pulsing electromagnetic fields. J Bone Joint Surg. 1982; 64: 888–895.
5. Matsunaga S. Histological and histochemical investigations of constant direct current stimulated intramedullary callus. Nippon Seikeigeka Gakkai Zasshi. 1986; 60: 1293–1330.
6. Aaron RK, Lennox D, Bunce GE, et al. The conservative treatment of osteonecrosis of the femoral head: a comparison of core decompression and pulsing electromagnetic fields. Clin Orthop. 1989; 249: 209–218.
7. Roberts WE. Bone tissue interface. Int J Oral Implantol. 1988; 5: 71–74.
8. Basset CAL, Mitchell S, Gaston SR. Results of treating 1, 078 ununited fractures and failed arthroses with pulsing electromagnetic fields. JAMA. 1982; 247: 623–628.
9. Adey WR. Tissue interactions with non-ionizing electromagnetic fields. Physio Rev. 1981; 61: 435–514.
10. Farndale RW, Murray JC. Pulsed electromagnetic fields promote collagen production in bone marrow fibroblasts via athermal mechanisms. Calcif Tissue Int. 1985; 37: 178–182.
11. Elliott JP, Smith RL, Block CA. Time-varying magnetic fields: Effects of orientation on chondrocyte proliferation. J Orthop Res. 1988; 6: 259–264.
12. Shimizu T, Zerwekh JE, Videman T, et al. Bone ingrowth into porous calcium phosphate ceramics: Influence of pulsing electromagnetic field. J Orthop Res. 1988; 6: 248–258.
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14. Buser D, Nydegger T, Oxland T, et al. Interface shear strength of titanium implants with a sandblasted and acid-etched surface: a biomechanical study in the maxilla of miniature pigs. J Biomed Mater Res. 1999; 45: 75–83.
15. Wennerberg A, Albrektsson T. Suggested guidelines for the topographic evaluation of implant surfaces. Int J Oral Maxillofac Implants. 2000; 15: 331–344.

Abstract Translations [German, Spanish, Portuguese, Japanese]

AUTOR(EN): Edmur Pereira BUZZA, DDS, MS*, Jamil Awad SHIBLI, DDS, MS**, Roberto Henrique BARBEIRO, DDS, MS, Ph.D.***, José Ricardo de Albergaria BARBOSA, DDS, MS, Ph.D.****. *Forschungsmitglied in der Abteilung für Gesichts- und Kieferchirurgie, zahnmedizinische Fakultät Piracicaba (UNICAMP), Piracicaba-SP, Brasilien; zurzeit: Professor für Gesichts- und Kieferchirurgie, Paulista Universität (UNIP) São José Rio Preto-SP, Brasilien. **Forschungsmitglied in der Abteilung für Orthodontie, zahnmedizinische Fakultät Araquara (UNESP), Araquara-SP, Brasilien. ***Professor für Gesichts- und Kieferchirurgie, zahnmedizinische Fakultät Araquara (UNESP), Araquara-SP, Brasilien. ****Professor für Gesichts- und Kieferchirurgie, zahnmedizinische Fakultät Piracicaba (UNICAMP), Piracicaba-SP, Brasilien. Schriftvehrker: Jamil Awad Shibli, DDS, MS, Periodontia, Faculdade de Odontologia de Araquara - UNESP, R. Humaitá, 1680, 14801 - 903 Araquara - SP, Brasilien. Telefon.: +55 16 201- 6369, Fax: +55 16 201 - 6314. eMail: perio@foar.unesp.br

ZUSAMMENFASSUNG: Zielsetzung: Diese Pilotstudie zielte darauf ab, die histologischen sowie mechanischen Komponenten innerhalb des durch Impulselektromagnetstrahlung (IEMS) unterstützten Heilungsprozesses beim Einsatz von Zahnimplantaten zu erfassen. Methoden und Materialien: Zur Versuchsdurchführung wurden 12 weiße Neuseeland-Hasen herangezogen, in deren Schienbeinmetaphyse insgesamt 48 Befestigungsimplantate aus reinem Titan eingepflanzt wurden. Die Versuchstiere wurden in eine Kontroll- und in eine Testgruppe (IEMS) aufgeteilt. Die Tiere der Testgruppe wurden täglich 30 Minuten lang einer Impulselektromagnetstrahlung mit einer Impulsbreite von 85 μs und einer Pulsfrequenz von 20 Mc ausgesetzt. Zur weiteren Untersuchung wurden die Tiere 21 bzw. 42 Tage nach erfolgter Implantation eingeschläfert. An allen Versuchstieren wurden die vorgesehenen mechanischen Tests durchgeführt; das Knochengewebe wurde zur Analyse der dekalzifizierten Bereiche durch Biopsie untersucht. Ergebnisse: Bezüglich der mechanischen Tests ergaben sich für die beiden Versuchsgruppen keine wesentlichen Ergebnisunterschiede (p>0,05). Berücksichtigt man allerdings den Zeitfaktor, konnten statistische Unterschiede ermittelt werden (p<0,0001). Die Untersuchung beider Gruppen wies ähnliche histologische Befunde auf. Schlussfolgerungen: Auf Basis der Versuchsergebnisse ist der Rückschluss zulässig, dass die Stimulation durch Impulselektromagnetstrahlung keinen wesentlichen Beitrag zur Heilung des die reinen Titanimplantate umlagernden Knochengewebes leistet.

SCHLÜSSELWÖRTER: Zahnimplantate, elektrische Stimulation, mechanische Tests, Integration des umliegenden Knochengewebes

Efectos del campo electromagnético en la curación del hueso alrededor de una superficie de titanio comercialmente puro: Estudio histológico y mecánico en conejos

AUTOR(ES): Edmur Pereira BUZZA, DDS, MS*, Jamil Awad SHIBLI, DDS, MS**, Roberto Henrique BARBEIRO, DDS, MS, Ph.D.***, José Ricardo de Albergaria BARBOSA, DDS, MS, Ph.D.†*Investigador del Departamento de Cirugía Oral y Maxilofacial, Facultad de Odontología de Piracicaba (UNICAMP), Piracicaba-SP, Brasil; Actualmente: Profesor del Departamento de Cirugía Oral, Universidad Paulista, Sao Jose Rio Preto-SP, Brasil. **Investigador del Departamento de Periodontología, Facultad de Odontología de Araraquara (UNESP), Araraquara-SP, Brasil. ***Profesor del Departamento de Cirugía Oral y Maxilofacial, Facultad de Odontología de Araraquara (UNESP), Araraquara-SP, Brasil. †Profesor del Departamento de Cirugía Oral y Maxilofacial, Facultad de Odontología de Piracicaba (UNICAMP), Piracicaba-SP, Brasil. Correspondencia a: Jamil Awad Shibli, DDS, MS, Periodontia, Faculdade de Odontologia de Araraquara UNESP, R. Humaitá 1680, 14801-903 Araraquara-SP, Brazil. Teléfono: + 55 16 201-6369, Fax + 55 16 201-6314. Correo electrónico: perio@foar.unesp.br

ABSTRACTO: PROPÓSITO: El propósito de este estudio piloto fue evaluar el proceso de curación histológica y mecánica en los implantes dentales bajo la acción de un campo electromagnético con pulsos (PEMF). MÉTODO Y MATERIALES: Cuarenta y ocho implantes de titanio comercialmente puro fueron implantados en la metafisis tibia de 12 conejos blancos de Nueva Zelanda divididos en el grupo de control y de prueba (PEMF). Un PEMF con una amplitud de impulso de 85 μs y una frecuencia del pulso de 20 Mc se aplicaron durante 30 minutos por día. Los animales fueron sacrificados 21 y 42 días después del implante. Las pruebas mecánicas se realizaron en todos los animales y se prepararon biopsias del hueso para completar análisis de secciones descalcificadas. RESULTADOS: Las pruebas mecánicas no demostraron diferencias significativas entre los grupos (p > 0,05). Sin embargo, se observaron diferencias estadísticas a través del tiempo (p > 0,0001). Las características histológicas similares se lograron para ambos grupos. CONCLUSIÓN: Estos resultados sugieren que la estimulación PEMF no mejora el proceso de curación del hueso alrededor de implantes dentales comercialmente puros.

PALABRAS CLAVES: Implantes dentales, estimulación eléctrica, pruebas mecánicas, integración ósea

Efeitos do campo eletromagnético na cicatrização óssea em redor da superfície de titânio puro: estudo histológico e mecânico em coelhos

AUTOR(ES): Edmur Pereira BUZZÁ, DDS, MS*, Jamil Awad SHIBLI, DDS, MS**, Roberto Henrique BARBEIRO, DDS, MS, Ph.D.*** e José Ricardo de Albergaria BARBOSA, DDS, MS, Ph.D. *Pesquisador do Departamento de Cirurgia Oral e Maxilofacial, Faculdade de Odontologia de Piracicaba (UNICAMP), Piracicaba, SP, Brasil; No presente: Professor do Departamento de Cirurgia Oral, Universidade Paulista (UNIP), São José do Rio Preto, SP, Brasil. ** Pesquisador do Departamento de Periodontologia, Faculdade de Odontologia de Araraquara (UNESP), Araraquara, SP, Brasil. *** Professor do Departamento de Cirurgia Oral e Maxilofacial, Faculdade de Odontologia de Araraquara (UNESP), Araraquara, SP, Brasil. đ Pesquisador do Departamento de Cirurgia Oral e Maxilofacial, Faculdade de Odontologia de Piracicaba (UNICAMP), Piracicaba, SP, Brasil. Correspondências devem ser enviadas a: Jamil Awad Shibili, DDS, MS. Periodontia, Faculdade de Odontologia de Araraquara-UNESP, R. Humaitá, 1680, 14801-903 Araraquara, SP, Brasil. Telefone: +55 16 201-6369, Fax: +55 16 201-6314. email: perio@foar.unesp.br

SINOPSE: Objetivo: a avaliação do processo de cicatrização histológica e mecânica em implantes odontológicos sob a ação do campo eletromagnético pulsátil (PEMF, ou pulsed electromagnetic field) foi o propósito geral deste projeto. Metodologia e materiais: quarenta e oito fixações de implante comercial puro foram implantados na metáfise da tíbia de 12 coelhos brancos neo-zelandeses, divididos em grupos de controle e teste (PEMF). Durante 30 minutos por dia aplicou-se um PEMF com largura de pulso de 85 μs e uma freqüência de pulso de 20 Mc. Os animais foram sacrificados 21 e 42 dias após a implantação. Os testes mecânicos foram realizados em todos os animais e foram preparadas biópsias ósseas para análise de seções descalcificadas. Resultados: os testes mecânicos não exibiram diferenças significativas entre os grupos (p>0,05). Entretanto, observaram-se diferenças estatísticas ao longo do tempo (p<0,0001). Alcançaram-se características histológicas similares para ambos os grupos. Conclusão: estes resultados sugerem que a estimulação por PEMF não aprimora o processo de cicatrização óssea em redor dos implantes odontológicos comercialmente puros.

PALAVRAS-CHAVES: implantes odontológicos, estimulação elétrica, testes mecânicos, osseointegração

FIGURE

Figure
Figure
Keywords:

dental implants; electrical stimulation; mechanical tests; osseointegration

© 2003 Lippincott Williams & Wilkins, Inc.